A meta-analysis of the strength and nature of cytoplasmic genetic effects

Journal of Evolutionary Biology

Volumn 27, Issue 10, 2014, Pages 2021-2034

  Dobler, R ^a   Rogell, B ^b   Budar, F ^c   Dowling, D K ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MONASH UNIVERSITY   (Australia)

^c INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

Chloroplast; Co adaptation; Co evolution; Cytoplasmic nuclear interaction; Life history; Mito nuclear interaction; Mitochondria

Indexed keywords

VASCONCELLEA CANDICANS;

ANIMAL; BIOLOGICAL MODEL; CELL NUCLEUS; CHLOROPLAST GENOME; CYTOPLASM; EVOLUTION; FEMALE; GENETIC VARIABILITY; GENETICS; MALE; META ANALYSIS; MITOCHONDRIAL GENOME; PHENOTYPE; PLANT; STATISTICAL MODEL;

ANIMALS; BIOLOGICAL EVOLUTION; CELL NUCLEUS; CYTOPLASM; FEMALE; GENETIC VARIATION; GENOME, CHLOROPLAST; GENOME, MITOCHONDRIAL; LINEAR MODELS; MALE; MODELS, GENETIC; PHENOTYPE; PLANTS;

EID: 84911986127     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12468     Document Type: Review

References (155)

1. Albert, B., Lelandais, C., Pla, M., Leuret, C., Vitart, E., Mathieu, C. et al. 2003. Amplification of Nicotiana sylvestris mitochondrial subgenomes is under nuclear control and is associated with phenotypic changes. Genetica 117: 17-25.
2. Arnqvist, G., Dowling, D.K., Eady, P., Gay, L., Tregenza, T., Tuda, M. et al. 2010. Genetic architecture of metabolic rate: environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution 64: 3354-3363.
3. Avise, J. 1986. Mitochondrial-DNA and the evolutionary genetics of higher animals. Philos. Trans. R. Soc. B 312: 325-342.
4. Aw, W.C., Correa, C.C., Clancy, D.J. & Ballard, J.W.O. 2011. Mitochondrial DNA variants in Drosophila melanogaster are expressed at the level of the organismal phenotype. Mitochondrion 11: 756-763.
5. Ballard, J.W.O. & James, A.C. 2004. Differential fitness of mitochondrial DNA in perturbation cage studies correlates with global abundance and population history in Drosophila simulans. Proc. Biol. Sci. 271: 1197-1201.
6. Ballard, J.W.O. & Pichaud, N. 2013. Mitochondrial DNA: more than an evolutionary bystander. Funct. Ecol. 28: 218-231.
7. Ballard, J.W.O. & Rand, D.M. 2005. The population biology of mitochondrial DNA and its phylogenetic implications. Annu. Rev. Ecol. Evol. Syst. 36: 621-642.
8. Ballard, J.W.O. & Whitlock, M.C. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13: 729-744.
9. Ballard, J.W.O., Melvin, R.G., Katewa, S.D. & Maas, K. 2007. Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution 61: 1735-1747.
10. Balloux, F., Handley, L.J.L., Jombart, T., Liu, H. & Manica, A. 2009. Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proc. Biol. Sci. 276: 3447-3455.
11. Bang, S.W., Mizuno, Y., Kaneko, Y., Matsuzawa, Y. & Bang, K.S. 2003. Production of intergeneric hybrids between the C3-C4 intermediate species Diplotaxis tenuifolia (L.) DC. and Raphanus sativus L. Breed. Sci. 53: 231-236.
12. Barreto, F.S. & Burton, R.S. 2013. Evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rRNA. Mol. Biol. Evol. 30: 310-314.
13. Bar-Yaacov, D., Blumberg, A. & Mishmar, D. 2012. Mitochondrial-nuclear co-evolution and its effects on OXPHOS activity and regulation. Biochim. Biophys. Acta 1819: 1107-1111.
14. Belliard, G., Pelletier, G., Vedel, F. & Quetier, F. 1978. Morphological-characteristics and chloroplast DNA distribution in different cytoplasmic parasexual hybrids of Nicotiana tabacum. Mol. Gen. Genet. 165: 231-237.
15. Belliard, G., Vedel, F. & Pelletier, G. 1979. Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 281: 401-403.
16. Berbec, A. 1994. Variation among offspring of alloplasmic tobacco Nicotiana tabacum L. cv 'Zamojska 4' with the cytoplasm of N. knightiana Goodspeed. Theor. Appl. Genet. 89: 127-132.
17. Birky, C.W. 2001. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu. Rev. Genet. 35: 125-148.
18. Blier, P.U., Dufresne, F. & Burton, R.S. 2001. Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17: 400-406.
19. Bogdanova, V.S. 2007. Inheritance of organelle DNA markers in a pea cross associated with nuclear-cytoplasmic incompatibility. Theor. Appl. Genet. 114: 333-339.
20. Bogdanova, V.S., Galieva, E.R. & Kosterin, O.E. 2009. Genetic analysis of nuclear-cytoplasmic incompatibility in pea associated with cytoplasm of an accession of wild subspecies Pisum sativum subsp. elatius (Bieb.) Schmahl. Theor. Appl. Genet. 118: 801-809.
21. Bonnett, H.T., Kofer, W., Hakansson, G. & Glimelius, K. 1991. Mitochondrial involvement in petal and stamen development studied by sexual and somatic hybridization of Nicotiana species. Plant Sci. 80: 119-130.
22. Budar, F. & Fujii, S. 2012. Cytonuclear adaptation in plants. Adv. Bot. Res. 63: 99-126.
23. Budar, F. & Roux, F. 2011. The role of organelle genomes in plant adaptation: time to get to work! Plant Signal Behav. 6: 635-639.
24. Budar, F., Touzet, P. & De Paepe, R. 2003. The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117: 3-16.
25. Burton, R.S. & Barreto, F.S. 2012. A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol. Ecol. 21: 4942-4957.
26. Camus, M.F., Clancy, D.J. & Dowling, D.K. 2012. Mitochondria, maternal inheritance, and male aging. Curr. Biol. 22: 1717-1721.
27. Caruso, C.M., Case, A.L. & Bailey, M.F. 2012. The evolutionary ecology of cytonuclear interactions in angiosperms. Trends Plant Sci. 17: 638-643.
28. Chatelain, E.H., Pichaud, N., Ballard, J.W.O., Tanguay, R.M., Morrow, G. & Blier, P.U. 2011. Functional conservatism among Drosophila simulans flies experiencing different thermal regimes and mitochondrial DNA introgression. J. Exp. Zool. B Mol. Dev. Evol. 316: 188-198.
29. Clancy, D.J. 2008. Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell 7: 795-804.
30. Clark, A.G. 1985. Natural-selection with nuclear and cytoplasmic transmission. II. tests with Drosophila from diverse populations. Genetics 111: 97-112.
31. Cohen, J. 1988. Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates, Hillsdale, New Jersey.
32. Correa, C.C., Aw, W., Melvin, R.G., Pichaud, N. & Ballard, J.W.O. 2012. Mitochondrial DNA variants influence mitochondrial bioenergetics in Drosophila melanogaster. Mitochondrion 12: 459-464.
33. Darracq, A., Varre, J.S. & Touzet, P. 2010. A scenario of mitochondrial genome evolution in maize based on rearrangement events. BMC Genomics 11: 233.
34. Davila, J.I., Arrieta-Montiel, M.P., Wamboldt, Y., Cao, J., Hagmann, J., Shedge, V. et al. 2011. Double-strand break repair processes drive evolution of the mitochondrial genome in arabidopsis. BMC Biol. 9: 64.
35. Del Re, A. 2013. compute.es: compute effect sizes. URL http://cran.r-project.org/web/packages/compute.es.
36. Dowling, D.K. 2014. Evolutionary perspectives on the links between mitochondrial genotype and disease phenotype. Biochim. Biophys. Acta 1840: 1393-1403.
37. Dowling, D.K. & Simmons, L.W. 2009. Reactive oxygen species as universal constraints in life-history evolution. Proc. Biol. Sci. 276: 1737-1745.
38. Dowling, D.K., Abiega, K.C. & Arnqvist, G. 2007a. Temperature-specific outcomes of cytoplasmic-nuclear interactions on egg-to-adult development time in seed beetles. Evolution 61: 194-201.
39. Dowling, D.K., Friberg, U. & Arnqvist, G. 2007b. A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle. J. Evol. Biol. 20: 2113-2125.
40. Dowling, D.K., Friberg, U., Hailer, F. & Arnqvist, G. 2007c. Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster. Genetics 175: 235-244.
41. Dowling, D.K., Nowostawski, A.L. & Arnqvist, G. 2007d. Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? J. Evol. Biol. 20: 358-368.
42. Dowling, D.K., Friberg, U. & Lindell, J. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23: 546-554.
43. Downie, S. & Palmer, J. 1992. Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Molecular Systematic of Plants (P.S. Soltis, D.E. Soltis & J.J. Doyle, eds), pp. 14-35. Springer US, New York.
44. Dufay, M. & Billard, E. 2012. How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Ann. Bot. 109: 505-519.
45. Dyall, S.D., Brown, M.T. & Johnson, P.J. 2004. Ancient invasions: from endosymbionts to organelles. Science 304: 253-257.
46. Edmands, S. & Burton, R.S. 1999. Cytochrome c oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear-nuclear or nuclear-cytoplasmic coadaptation. Evolution 53: 1972-1978.
47. Edmands, S., Northrup, S.L. & Hwang, A.S. 2009. Maladapted gene complexes within populations of the intertidal copepod Tigriopus californicus? Evolution 63: 2184-2192.
48. Ellison, C.K. & Burton, R.S. 2006. Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60: 1382-1391.
49. Ellison, C.K. & Burton, R.S. 2008. Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62: 631-638.
50. Elson, J.L., Turnbull, D.M. & Howell, N. 2004. Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am. J. Hum. Genet. 74: 229-238.
51. Frank, S.A. & Hurst, L.D. 1996. Mitochondria and male disease. Nature 383: 224.
52. Friberg, U. & Dowling, D.K. 2008. No evidence of mitochondrial genetic variation for sperm competition within a population of Drosophila melanogaster. J. Evol. Biol. 21: 1798-1807.
53. Galloway, L.F. & Fenster, C.B. 1999. The effect of nuclear and cytoplasmic genes on fitness and local adaptation in an annual legume, Chamaecrista fasciculata. Evolution 53: 1734-1743.
54. Galtier, N., Nabholz, B., Glemin, S. & Hurst, G.D.D. 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol. Ecol. 18: 4541-4550.
55. Galun, E., Arzeegonen, P., Fluhr, R., Edelman, M. & Aviv, D. 1982. Cytoplasmic hybridization in Nicotiana - mitochondrial DNA analysis in progenies resulting from fusion between protoplasts having different organelle constitutions. Mol. Gen. Genet. 186: 50-56.
56. Gemmell, N.J., Metcalf, V.J. & Allendorf, F.W. 2004. Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol. Evol. 19: 238-244.
57. Gershoni, M., Templeton, A.R. & Mishmar, D. 2009. Mitochondrial bioenergetics as a major motive force of speciation. BioEssays 31: 642-650.
58. Gould, S.B., Waller, R.R. & McFadden, G.I. 2008. Plastid evolution. Annu. Rev. Plant Biol. 59: 491-517.
59. Gray, M.W., Burger, G. & Lang, B.F. 1999. Mitochondrial evolution. Science 283: 1476-1481.
60. Green, B.R. 2011. Chloroplast genomes of photosynthetic eukaryotes. Plant J. 66: 34-44.
61. Greiner, S. & Bock, R. 2013. Tuning a menage a trois: co-evolution and co-adaptation of nuclear and organellar genomes in plants. BioEssays 35: 354-365.
62. Greiner, S., Rauwolf, U., Meurer, J. & Herrmann, R.G. 2011. The role of plastids in plant speciation. Mol. Ecol. 20: 671-691.
63. Hadfield, J.D. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33: 1-22.
64. Hedges, L. 1981. Distribution theory for Glass's estimator of effect size and related estimators. J. Educ. Behav. Stat. 6: 107-128.
65. Hereford, J., Hansen, T.F. & Houle, D. 2004. Comparing strengths of directional selection: how strong is strong? Evolution 58: 2133-2143.
66. Hohmann-Marriott, M.F. & Blankenship, R.E. 2011. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62: 515-548.
67. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
68. Hurst, G.D.D. & Jiggins, F.M. 2005. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. Biol. Sci. 272: 1525-1534.
69. Iida, S., Miyagi, A., Aoki, S., Ito, M., Kadono, Y. & Kosuge, K. 2009. Molecular adaptation of rbcL in the heterophyllous aquatic plant Potamogeton. PLoS ONE 4: e4633.
70. Innocenti, P., Morrow, E.H. & Dowling, D.K. 2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332: 845-848.
71. James, A.C. & Ballard, J.W.O. 2003. Mitochondrial genotype affects fitness in Drosophila simulans. Genetics 164: 187-194.
72. Jones, P., Keane, E.M. & Osborne, B.A. 1998. Effects of alien cytoplasmic variation on carbon assimilation and productivity in wheat. J. Exp. Bot. 49: 1519-1528.
73. Kapralov, M.V., Kubien, D.S., Andersson, I. & Filatov, D.A. 2011. Changes in Rubisco kinetics during the evolution of C4 photosynthesis in Flaveria (Asteraceae) are associated with positive selection on genes encoding the enzyme. Mol. Biol. Evol. 28: 1491-1503.
74. Kingsolver, J.G., Diamond, S.E., Siepielski, A.M. & Carlson, S.M. 2012. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol. Ecol. 26: 1101-1118.
75. Kitazaki, K. & Kubo, T. 2010. Cost of having the largest mitochondrial genome: evolutionary mechanism of plant mitochondrial genome. J. Bot. 2010: 1-12.
76. Kivisild, T., Shen, P.D., Wall, D.P., Do, B., Sung, R., Davis, K. et al. 2006. The role of selection in the evolution of human mitochondrial genomes. Genetics 172: 373-387.
77. Kleine, T., Maier, U.G. & Leister, D. 2009. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu. Rev. Plant Biol. 60: 115-138.
78. Knoop, V. 2004. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr. Genet. 46: 123-139.
79. Koonin, E.V. 2010. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 11: 209.
80. Kubo, T. & Mikami, T. 2007. Organization and variation of angiosperm mitochondrial genome. Physiol. Plant. 129: 6-13.
81. Lambrides, C.J., Chapman, S.C. & Shorter, R. 2004. Genetic variation for carbon isotope discrimination in sunflower: association with transpiration efficiency and evidence for cytoplasmic inheritance. Crop Sci. 44: 1642-1653.
82. Lane, N. & Martin, W. 2010. The energetics of genome complexity. Nature 467: 929-934.
83. Leinonen, P.H., Remington, D.L. & Savolainen, O. 2011. Local adaptation, phenotypic differentiation, and hybrid fitness in diverged natural populations of Arabidopsis Lyrata. Evolution 65: 90-107.
84. Leinonen, P.H., Remington, D.L., Leppala, J. & Savolainen, O. 2013. Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Mol. Ecol. 22: 709-723.
85. Leppala, J. & Savolainen, O. 2011. Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsis lyrata subspecies. Evolution 65: 2959-2972.
86. Levin, D.A. 2003. The cytoplasmic factor in plant speciation. Syst. Bot. 28: 5-11.
87. Lewis, D. 1941. Male sterility in natural populations of hermaphrodite plants. New Phytol. 40: 56-63.
88. Liau, W.S., Gonzalez-Serricchio, A.S., Deshommes, C., Chin, K. & LaMunyon, C.W. 2007. A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genet. 8: 8.
89. Linke, B. & Borner, T. 2005. Mitochondrial effects on flower and pollen development. Mitochondrion 5: 389-402.
90. Lynch, M. 1997. Mutation accumulation in nuclear, organelle, and prokaryotic transfer RNA genes. Mol. Biol. Evol. 14: 914-925.
91. Lynch, M., Koskella, B. & Schaack, S. 2006. Mutation pressure and the evolution of organelle genomic architecture. Science 311: 1727-1730.
92. Maklakov, A.A., Friberg, U., Dowling, D.K. & Arnqvist, G. 2006. Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster. Evolution 60: 2081-2086.
93. McCauley, D.E. 1995. The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends Ecol. Evol. 10: 198-202.
94. McKay, J.K., Richards, J.H., Nemali, K.S., Sen, S., Mitchell-Olds, T., Boles, S. et al. 2008. Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, Kas-1 x Tsu-1. Evolution 62: 3014-3026.
95. Meiklejohn, C.D., Holmbeck, M.A., Siddiq, M.A., Abt, D.N., Rand, D.M. & Montooth, K.L. 2013. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9: e1003238.
96. Melvin, R.G. & Ballard, J.W.O. 2006. Intraspecific variation in survival and mitochondrial oxidative phosphorylation in wild-caught Drosophila simulans. Aging Cell 5: 225-233.
97. Messina, F.J. & Jones, J.C. 2011. Inheritance of traits mediating a major host shift by a seed beetle, Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Ann. Entomol. Soc. Am. 104: 808-815.
98. Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A.G., Hosseini, S. et al. 2003. Natural selection shaped regional mtDNA variation in humans. Proc. Natl. Acad. Sci. USA 100: 171-176.
99. Moison, M., Roux, F., Quadrado, M., Duval, R., Ekovich, M., Le, D.H. et al. 2010. Cytoplasmic phylogeny and evidence of cyto-nuclear co-adaptation in Arabidopsis thaliana. Plant J. 63: 728-738.
100. Montooth, K.L., Meiklejohn, C.D., Abt, D.N. & Rand, D.M. 2010. Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila. Evolution 64: 3364-3379.
101. Moran, N.A. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93: 2873-2878.
102. Moran, J.L. & Rooney, W.L. 2003. Effect of cytoplasm on the agronomic performance of grain Sorghum hybrids. Crop Sci. 43: 777-781.
103. Morrissey, M.B. & Hadfield, J.D. 2012. Directional selection in temporally replicated studies is remarkably consistent. Evolution 66: 435-442.
104. Mower, J.P., Touzet, P., Gummow, J.S., Delph, L.F. & Palmer, J.D. 2007. Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol. Biol. 7: 7.
105. Mukai, Y. & Tsunewaki, K. 1979. Basic studies on hybrid wheat breeding. VIII. A new male sterility-fertility restoration system in common wheat utilizing the cytoplasms of Aegilops kotschyi and Ae. variabilis. Theor. Appl. Genet. 54: 153-160.
106. Muller, H.J. 1932. Some genetic aspects of sex. Am. Nat. 66: 118-138.
107. Murai, K. 1997. Effects of Aegilops crassa cytoplasm on the agronomic characters in photoperiod-sensitive cms wheat lines and F1 hybrids. Breed. Sci. 47: 321-326.
108. Nakada, K., Sato, A., Yoshida, K., Morita, T., Tanaka, H., Inoue, S.I. et al. 2006. Mitochondria-related male infertility. Proc. Natl. Acad. Sci. USA 103: 15148-15153.
109. Newton, A.C., Allnutt, T.R., Gillies, A.C.M., Lowe, A.J. & Ennos, R.A. 1999. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol. Evol. 14: 140-145.
110. Nigro, L. 1994. Nuclear background affects frequency dynamics of mitochondrial DNA variants in Drosophila simulans. Heredity 72: 582-586.
111. Palmer, J.D. 1990. Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 6: 115-120.
112. Palmer, R.G. 1992. Conditional lethality involving a cytoplasmic mutant and chlorophyll-deficient malate-dehydrogenase mutants in soybean. Theor. Appl. Genet. 85: 389-393.
113. Palmer, R.G. & Decianzio, S.R. 1985. Conditional lethality involving nuclear and cytoplasmic chlorophyll mutants in soybeans. Theor. Appl. Genet. 70: 349-354.
114. Palmer, J.D. & Herbon, L.A. 1988. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28: 87-97.
115. Perrot-Minnot, M.J., Migeon, A. & Navajas, M. 2004. Intergenomic interactions affect female reproduction: evidence from introgression and inbreeding depression in a haplodiploid mite. Heredity 93: 551-558.
116. Perry, W.L., Feder, J.L., Dwyer, G. & Lodge, D.M. 2001. Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution 55: 1153-1166.
117. Pershina, L.A., Rakovtseva, T.S., Belova, L.I., Devyatkina, E.P., Silkova, O.G., Kravtsova, L.A. et al. 2007. Effect of rye Secale cereale L. chromosomes 1R and 3R on polyembryony expression in hybrid combinations between (Hordeum L.)- Triticum aestivum L. alloplasmic recombinant lines and wheat T. aestivum L.-rye S. cereale L. substitution lines. Russ. J. Genet. 43: 791-797.
118. Pichaud, N., Ballard, J.W.O., Tanguay, R.M. & Blier, P.U. 2012. Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: insight into functional properties of mitochondria. Evolution 66: 3189-3197.
119. Pichaud, N., Ballard, J.W.O., Tanguay, R.M. & Blier, P.U. 2013. Mitochondrial haplotype divergences affect specific temperature sensitivity of mitochondrial respiration. J. Bioenerg. Biomembr. 45: 25-35.
120. Planchart, A., You, Y. & Schimenti, J.C. 2000. Physical mapping of male fertility and meiotic drive quantitative trait loci in the mouse t complex using chromosome deficiencies. Genetics 155: 803-812.
121. Price, T. & Schluter, D. 1991. On the low heritability of life-history traits. Evolution 45: 853-861.
122. Provan, J., Powell, W. & Hollingsworth, P.M. 2001. Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol. Evol. 16: 142-147.
123. R Development Core Team 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org.
124. Rai, K.N. 1995. A new cytoplasmic-nuclear male sterility system in pearl millet. Plant Breeding 114: 445-447.
125. Rai, K.N., Virk, D.S., Harinarayana, G. & Rao, A.S. 1996. Stability of male-sterile sources and fertility restoration of their hybrids in pearl millet. Plant Breeding 115: 494-500.
126. Rand, D.M., Clark, A.G. & Kann, L.M. 2001. Sexually antagonistic cytonuclear fitness interactions in Drosophila melanogaster. Genetics 159: 173-187.
127. Rand, D.M., Haney, R.A. & Fry, A.J. 2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19: 645-653.
128. Rand, D.M., Fry, A. & Sheldahl, L. 2006. Nuclear-mitochondrial epistasis and Drosophila aging: introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics 172: 329-341.
129. Rawson, P.D. & Burton, R.S. 2002. Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc. Natl. Acad. Sci. USA 99: 12955-12958.
130. Reddy, P.S., Rao, D.M., Reddy, V.S.B. & Kumar, A.A. 2010. Inheritance of male-fertility restoration in A1, A2, A3 and A4(M) cytoplasmic male-sterility systems of sorghum [Sorghum bicolor (L.) Moench]. Indian J. Genet. Plant Breed. 70: 240-246.
131. Reinhardt, K., Dowling, D.K. & Morrow, E.H. 2013. Mitochondrial replacement, evolution, and the clinic. Science 341: 1345-1346.
132. Rosenthal, J.A. 1996. Qualitative descriptors of strength of association and effect size. J. Soc. Serv. Res. 21: 37-59.
133. Ruiz-Pesini, E., Mishmar, D., Brandon, M., Procaccio, V. & Wallace, D.C. 2004. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223-226.
134. Sambatti, J.B.M., Ortiz-Barrientos, D., Baack, E.J. & Rieseberg, L.H. 2008. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11: 1082-1091.
135. Sattari, M., Kathiresan, A., Gregorio, G.B. & Virmani, S.S. 2008. Comparative genetic analysis and molecular mapping of fertility restoration genes for WA, Dissi, and Gambiaca cytoplasmic male sterility systems in rice. Euphytica 160: 305-315.
136. Saxena, K.B., Sultana, R., Saxena, R.K., Kumar, R.V., Sandhu, J.S., Rathore, A. et al. 2011. Genetics of fertility restoration in A4-based, diverse maturing hybrids of pigeonpea [Cajanus cajan (L.) Millsp.]. Crop Sci. 51: 574-578.
137. Scotti, N., Monti, L. & Cardi, T. 2003. Organelle DNA variation in parental Solanum spp. genotypes and nuclear-cytoplasmic interactions in Solanum tuberosum (+) S. commersonii somatic hybrid-backcross progeny. Theor. Appl. Genet. 108: 87-94.
138. Shykoff, J.A., Kolokotronis, S.O., Collin, C.L. & Lopez-Villavicencio, M. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9.
139. Sloan, D.B., Barr, C.M., Olson, M.S., Keller, S.R. & Taylor, D.R. 2008. Evolutionary rate variation at multiple levels of biological organization in plant mitochondrial DNA. Mol. Biol. Evol. 25: 243-246.
140. Sloan, D.B., Alverson, A.J., Chuckalovcak, J.P., Wu, M., McCauley, D.E., Palmer, J.D. et al. 2012a. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 10: e1001241.
141. Sloan, D.B., Muller, K., McCauley, D.E., Taylor, D.R. & Storchova, H. 2012b. Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol. 196: 1228-1239.
142. Smith, S., Turbill, C. & Suchentrunk, F. 2010. Introducing mother's curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares. Mol. Ecol. 19: 36-43.
143. Song, K., Tang, K. & Osborn, T.C. 1993. Development of synthetic Brassica amphidiploids by reciprocal hybridization and comparison to natural amphidiploids. Theor. Appl. Genet. 86: 811-821.
144. Sun, C., Kong, Q.P. & Zhang, Y.P. 2007. The role of climate in human mitochondrial DNA evolution: a reappraisal. Genomics 89: 338-342.
145. Takeda, K., Tasai, M., Iwamoto, M., Onishi, A., Tagami, T., Nirasawa, K. et al. 2005. Microinjection of cytoplasm or mitochondria derived from somatic cells affects parthenogenetic development of murine oocytes. Biol. Reprod. 72: 1397-1404.
146. Takeda, K., Tasai, M., Akagi, S., Matsukawa, K., Takahashi, S., Iwamoto, M. et al. 2010. Microinjection of serum-starved mitochondria derived from somatic cells affects parthenogenetic development of bovine and murine oocytes. Mitochondrion 10: 137-142.
147. Tang, Z.X., Yang, Z.F., Hu, Z.Q., Zhang, D., Lu, X., Jia, B. et al. 2013. Cytonuclear epistatic quantitative trait locus mapping for plant height and ear height in maize. Mol. Breed. 31: 1-14.
148. Tao, D.Y., Hu, F.Y., Yang, J.Y., Yang, G.F., Yang, Y.Q., Xu, P. et al. 2004. Cytoplasm and cytoplasm-nucleus interactions affect agronomic traits in japonica rice. Euphytica 135: 129-134.
149. Unckless, R.L. & Herren, J.K. 2009. Population genetics of sexually antagonistic mitochondrial mutants under inbreeding. J. Theor. Biol. 260: 132-136.
150. Vavre, F., Fleury, F., Varaldi, J., Fouillet, P. & Bouletreau, M. 2000. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution 54: 191-200.
151. Verma, J.K., Sodhi, Y.S., Mukhopadhyay, A., Arumugam, N., Gupta, V., Pental, D. et al. 2000. Identification of stable maintainer and fertility restorer lines for 'Polima' CMS in Brassica campestris. Plant Breeding 119: 90-92.
152. Williams, H.L. & Fenster, C.B. 1998. Ecological and genetic factors contributing to the low frequency of male sterility in Chamaecrista fasciculata (Fabaceae). Am. J. Bot. 85: 1243-1250.
153. Wolff, J., Ladoukakis, E., Enrríquez, J. & Dowling, D. 2014. Mito-nuclear interactions - evolutionary consequences over multiple biological scales. Philos. Trans. R. Soc. B 369: 20130443.
154. Yee, W.K.W., Sutton, K.L. & Dowling, D.K. 2013. In vivo male fertility is affected by naturally occurring mitochondrial haplotypes. Curr. Biol. 23: R55-R56.
155. Zubko, M.K., Zubko, E.I. & Gleba, Y.Y. 2002. Self-fertile cybrids Nicotiana tabacum (+Hyoscyamus aureus) with a nucleo-plastome incompatibility. Theor. Appl. Genet. 105: 822-828.